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Bacillus Telluris Sp. Nov. Isolated from Greenhouse Soil in Beijing, China

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Bacillus Telluris Sp. Nov. Isolated from Greenhouse Soil in Beijing, China microorganisms Article Bacillus telluris sp. nov. Isolated from Greenhouse Soil in Beijing, China He-Bao Guo, Shan-Wen He , Xing Wang, Kyu-Kyu Thin, Hai-Lei Wei * and Xiao-Xia Zhang * Key Laboratory of Microbial Resources Collection and Preservation, Ministry of Agriculture and Rural Affairs, Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural Sciences, Beijing 100081, China; [email protected] (H.-B.G.); [email protected] (S.-W.H.); [email protected] (X.W.); [email protected] (K.-K.H.) * Correspondence: [email protected] (H.-L.W.); [email protected] (X.-X.Z.) Received: 28 February 2020; Accepted: 8 May 2020; Published: 10 May 2020 Abstract: A novel Gram-stain-positive, rod-shaped, endospore-forming bacterium, which we designated as strain 03113T, was isolated from greenhouse soil in Beijing, China. Phylogenetic analysis based on 16S rRNA gene sequences showed strain 03113T is in the genus Bacillus and had T the highest similarity to Bacillus solani CCTCC AB 2014277 (98.14%). The strain grew at 4 ◦C–50 ◦C (optimum 37 ◦C), with 0–10% (w/v) NaCl (optimum 5%), and in the range of pH 3.0–12.0 (optimum pH 8.0). Menaquinone was identified as MK-7, and the major polar lipids were diphosphatidylglycerol, phosphatidylglycerol, and phosphatidylethanolamine. The main major cellular fatty acids detected were anteiso-C15:0 (51.35%) and iso-C15:0 (11.06%), which are the predominant cellular fatty acids found in all recognized members of the genus Bacillus. The 16S rRNA gene sequence and core-genome analysis, the average nucleotide identity (ANI), and in silico DNA—DNA hybridization (DDH) value between strain 03113T and the most closely related species were 70.5% and 22.6%, respectively, which supported our conclusion that 03113T represented a novel species in the genus Bacillus. We demonstrated that type strain 03113T (=ACCC 03113T=JCM 33017T) was a novel species in the genus Bacillus, and the name Bacillus telluris sp. nov. was proposed. Strain 03113T secreted auxin IAA and carried the nitrogenase iron protein (nifH) gene, which indicated that strain 03113T has the potential to fix nitrogen and promote plant growth. Bacillus telluris sp. nov. 03113T is a potential candidate for the biofertilizers of organic agriculture areas. Keywords: Bacillus telluris sp. nov.; genome analysis; plant-growth promoting rhizobacterium 1. Introduction The genus Bacillus was first described by Cohn in 1872, and it is a genus of ubiquitous soil microorganisms [1]. It is comprised of endospore-forming, rod-shaped bacteria that are members of the phylum Firmicutes [2]. At the time of writing, there were 379 species in the genus Bacillus recorded on LPSN (www.bacterio.net/bacillus.html; Nov 2019). Based on their genetic similarity, Bacillus species can be classified into several groups, which include Bacillus cereus–Bacillus anthracis–Bacillus thuringiensis, Bacillus clausii–Bacillus halodurans, Bacillus coahuilensis–Bacillus sp. NRRLB-14911, and Bacillus subtilis–Bacillus licheniformis–Bacillus pumilus [3]. In addition, species in the genus Bacillus have a wide range of physiological and biochemical characteristics from psychrophilic to thermophilic, acidophilic to alkaliphilic, and some are halophilic [4], which allow them to live in a wide range of extreme habitats, such as desert sands, hot springs, and Arctic soils. In addition, the genus Bacillus is an extremely diverse group of bacteria that includes both the causative agent of anthrax (B. anthracis)[5,6] and several species that synthesize important antibiotics. In addition to medical uses, bacillus spores, due to their extreme tolerance of both heat and disinfectants, are used to test heat sterilization techniques Microorganisms 2020, 8, 702; doi:10.3390/microorganisms8050702 www.mdpi.com/journal/microorganisms Microorganisms 2020, 8, 702 2 of 11 and chemical disinfectants. Bacilli are also used in the detergent manufacturing industry for their ability to synthesize important enzymes. In this study, we report a novel bacterial strain, 03113T, which was isolated from the greenhouse soil of Wangsiying, Chaoyang District, Beijing, China. Based on the phenotypic characteristics and phylogenetic analysis, strain 03113T represents a novel species in the genus Bacillus. 2. Materials and Methods 2.1. Bacterial Strains, Growth Conditions, and Cultivation Strain 03113T was isolated from greenhouse soil from Wangsiying, Chaoyang District, Beijing, China (40◦090N, 116◦420E). We preserved the sample in freeze-dried milk ampoules at 4 ◦C and 20% (v/v) glycerol at 80 C[7]. The type strains of species closely related to strain 03113T were used as − ◦ reference strains under the same conditions for comparative taxonomic analysis, which included B. T T T solani CCTCC AB 2014277 , B. praedii CCTCC AB 2015208 , and B. dabaoshanensis CCTCC AB 2013260 . TM All strains were maintained and cultivated in TSA or TSB (Difco ) medium plates at 30 ◦C, unless otherwise stated. 2.2. Phenotypic Characterization Biochemical characteristics of strain 03113T were investigated. Growth at eight different temperatures (4, 15, 25, 30, 37, 40, 45, and 50 ◦C) was tested on TSA plates. The pH values (pH 3.0, 4.0, 5.0, 6.0, 7.0, 8.0, 9.0, 10.0, 11.0, and 12.0, with increments of 1.0 pH unit) were tested in LB medium. Growth at various NaCl concentrations was tested over the range 0% 12% (w/v) NaCl (at intervals of 1%) − by incubating at 30 ◦C[8]. Gram staining was performed using the Gram-stain kit [9]. Cell morphology was observed by light microscopy (CX21; Olympus) and transmission electron microscopy. Endospores were examined according to the Schaeffer–Fulton staining method [10]. Motility was examined on motility agar [11]. Catalase activity was determined by investigating bubble production with 3% (v/v) H2O2, and oxidase activity was determined using 1% (v/v) tetramethyl-p-phenylenediamine. The basic biochemical characteristics were investigated on API-20NE, API 50CH (BioMérieux) [12], and BIOLOG GEN III MicroPlate (BIOLOG), according to the manufacturer’s instructions. The type strains of B. solani CCTCC AB 2014277T, B. praedii CCTCC AB 2015208T, and B. dabaoshanensis CCTCC AB 2013260T were used as reference strains. 2.3. Chemotaxonomic Analysis For the measurement of chemotaxonomic characteristics, the menaquinone system was analyzed as described by Collins et al. [13] using reversed-phase HPLC [14]. The analysis of polar lipids by two-dimensional TLC was performed according to the method described by Minnikin et al. [15]. The cellular fatty acid is a useful and functional tool to identify species in the genus Bacillus and related genera. After 48 h of incubation at 30 ◦C on TSA, cellular fatty acids were extracted and analyzed using the method described by Sasser [16] and identified with the MIDI Sherlock Microbial Identification System (Library RTSA6 6.0, MIDI Sherlock Software Package, Version 6.0; Agilent 6890N). 2.4. Phylogenetic 16S rRNA Gene Analysis Genomic DNA was extracted from a single colony of the novel strain grown on TSA plates at 30 ◦C for 2 d using Bacteria DNA Kit (Tiangen, Beijing, China), according to the manufacturer’s protocol. The 16S rRNA gene was amplified by PCR and sequenced using the universal primers 27F(5’-AGAGTTTGATCCTGGCTCAG-3’) and 1492R(5’-GGTTACCTTGTTACGACTT-3’) [17]. Pairwise 16S rRNA gene sequence similarities were calculated using the EzTaxon-e database (http://eztaxon-e.ezbiocloud.net/)[18]. The CLUSTAL_W algorithm was used for sequence alignments using the neighbour-joining [19,20] and maximum-likelihood [21] methods that were implemented with Mega 7.0 software for phylogenetic analysis. Evolutionary distances were computed by using Microorganisms 2020, 8, 702 3 of 11 the Kimura two-parameter model [22]. The robustness of the tree branches was estimated by bootstrap analysis with 1000 replications [23]. The GenBank/EMBL/DDBJ accession number of 16S rRNA sequence is MN907472. 2.5. Complete Genome Sequencing and Analysis To confirm the results of the 16S rRNA gene sequence similarity analysis, the complete genome sequence of the novel species was performed. The genome was sequenced by Personal Biotechnology Co., Ltd (Shanghai, PR China). Genomes of the most closely related species chosen above were retrieved from the GenBank database in NCBI. Reads of each data set were filtered by using AdapterRemoval (ver. 2.1.7) [24], and high-quality paired-end reads were assembled using A5-MiSeq v20150522 [25]. The open reading frames (ORFs) were predicted by GeneMarkS (ver. 4.32 April 2015) [26]. The tRNA genes were predicted by tRNAscan-SE 94 (ver. 1.3.1) and the rRNA genes by Barrnap (0.9-dev) 95 (https://github.com/tseemann/barrnap)[27]. Calculations of average nucleotide identity (ANI) were performed using JSpecies software (http://www.imedea.uib.es/jspecies). In silico DNA—DNA hybridization (DDH) estimates were performed using Genome-to-Genome Distance Calculator (GGDC) with the BLAST+ (recommended) method [28]. The partial genome files were uploaded to the GGDC 2.0 web interface (http://ggdc.dsmz.de/ggdc.php#), and Formula 2 was used as recommended for the calculation of DDH values. As a further extension of genome-based phylogeny, the GGDC website was used to establish the phylogenomic tree of strain 03113T and other closely related Bacillus species. 2.6. Analysis of Core Orthologous Genes To identify orthologous genes among the strains in Bacillus species, 13 Bacillus strains were selected for the core genome analysis based on their biological control properties. The 13 bacteria included B. solani CCTCC AB 2014277T, B. praedii CCTCC AB 2015208T, B. glycinifermentans GO-13, B. acidicola FJAT-2406, B. salacetis SKP7-4, B. shackletonii LMG 18435, B. circulans NBRC 13626, B. foraminis Bac44, B. persicus DSM 25386, B. oceanisediminis CGMCC 1.10115, B. firmus NCTC 10335, B. gottheilii FJAT-2394, and 03113T. The Bacterial Pan Genome Analysis (BPGA) pipeline [29] was used for the pan-genome analyses. The clustering tool USEARCH was used to cluster protein families.
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